Skip to main content

Advertisement

Log in

Impact of Cerebral Autoregulation Monitoring in Cerebrovascular Disease: A Systematic Review

  • Review Article
  • Published:
Neurocritical Care Aims and scope Submit manuscript

Abstract

Cerebral autoregulation (CA) prevents brain injury by maintaining a relatively constant cerebral blood flow despite fluctuations in cerebral perfusion pressure. This process is disrupted consequent to various neurologic pathologic processes, which may result in worsening neurologic outcomes. Herein, we aim to highlight evidence describing CA changes and the impact of CA monitoring in patients with cerebrovascular disease, including ischemic stroke, intracerebral hemorrhage (ICH), and aneurysmal subarachnoid hemorrhage (aSAH). The study was preformed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines. English language publications were identified through a systematic literature conducted in Ovid Medline, PubMed, and Embase databases. The search spanned the dates of each database’s inception through January 2021. We selected case–control studies, cohort observational studies, and randomized clinical trials for adult patients (≥ 18 years) who were monitored with continuous metrics using transcranial Doppler, near-infrared spectroscopy, and intracranial pressure monitors. Of 2799 records screened, 48 studies met the inclusion criteria. There were 23 studies on ischemic stroke, 18 studies on aSAH, 5 studies on ICH, and 2 studies on systemic hypertension. CA impairment was reported after ischemic stroke but generally improved after tissue plasminogen activator administration and successful mechanical thrombectomy. Persistent impairment in CA was associated with hemorrhagic transformation, malignant cerebral edema, and need for hemicraniectomy. Studies that investigated large ICHs described bilateral CA impairment up to 12 days from the ictus, especially in the presence of small vessel disease. In aSAH, impairment of CA was associated with angiographic vasospasm, delayed cerebral ischemia, and poor functional outcomes at 6 months. This systematic review highlights the available evidence for CA disruption during cerebrovascular diseases and its possible association with long-term neurological outcome. CA may be disrupted even before acute stroke in patients with untreated chronic hypertension. Monitoring CA may help in establishing individualized management targets in patients with cerebrovascular disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Lassen NA. Cerebral blood flow and oxygen consumption in man. Physiol Rev. 1959;39(2):183–238.

    Article  CAS  PubMed  Google Scholar 

  2. Haggendal E, Johansson B. Effects of arterial carbon dioxide tension and oxygen saturation on cerebral blood flow autoregulation in dogs. Acta Physiol Scand Suppl. 1965;258:27–53.

    Article  CAS  PubMed  Google Scholar 

  3. Moyer JH, Morris G. Cerebral hemodynamics during controlled hypotension induced by the continuous infusion of ganglionic blocking agents (hexamethonium, pendiomide and arfonad). J Clin Invest. 1954;33(8):1081–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Olsen KS, Svendsen LB, Larsen FS, Paulson OB. Effect of labetalol on cerebral blood flow, oxygen metabolism and autoregulation in healthy humans. Br J Anaesth. 1995;75(1):51–4.

    Article  CAS  PubMed  Google Scholar 

  5. Drummond JC. The lower limit of autoregulation: time to revise our thinking? Anesthesiology. 1997;86(6):1431–3.

    Article  CAS  PubMed  Google Scholar 

  6. Deeks JJ, Dinnes J, D’Amico R, et al. Evaluating non-randomised intervention studies. Health Technol Assess. 2003;7(27):1–173.

    Article  Google Scholar 

  7. Yang SH. Primer on cerebrovascular diseases. 2nd ed. Amsterdam: Elseiver Inc.; 2017.

    Google Scholar 

  8. Armstead WM. Cerebral blood flow autoregulation and dysautoregulation. Anesthesiol Clin. 2016;34(3):465–77.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Sen AN, Gopinath SP, Robertson CS. Clinical application of near-infrared spectroscopy in patients with traumatic brain injury: a review of the progress of the field. Neurophotonics. 2016;3(3):031409.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Budohoski KP, Zweifel C, Kasprowicz M, et al. What comes first? The dynamics of cerebral oxygenation and blood flow in response to changes in arterial pressure and intracranial pressure after head injury. Br J Anaesth. 2012;108(1):89–99.

    Article  CAS  PubMed  Google Scholar 

  11. Czosnyka M, Smielewski P, Kirkpatrick P, Laing RJ, Menon D, Pickard JD. Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery. 1997;41(1):11–7.

    Article  CAS  PubMed  Google Scholar 

  12. Bouma GJ, Muizelaar JP, Bandoh K, Marmarou A. Blood pressure and intracranial pressure-volume dynamics in severe head injury: relationship with cerebral blood flow. J Neurosurg. 1992;77(1):15–9.

    Article  CAS  PubMed  Google Scholar 

  13. Rivera-Lara L, Zorrilla-Vaca A, Geocadin R, et al. Predictors of outcome with cerebral autoregulation monitoring: a systematic review and meta-analysis. Crit Care Med. 2017;45(4):695–704.

    Article  PubMed  Google Scholar 

  14. Bishop CC, Powell S, Rutt D, Browse NL. Transcranial Doppler measurement of middle cerebral artery blood flow velocity: a validation study. Stroke. 1986;17(5):913–5.

    Article  CAS  PubMed  Google Scholar 

  15. Larsen FS, Olsen KS, Hansen BA, Paulson OB, Knudsen GM. Transcranial Doppler is valid for determination of the lower limit of cerebral blood flow autoregulation. Stroke. 1994;25(10):1985–8.

    Article  CAS  PubMed  Google Scholar 

  16. Reinhard M, Roth M, Muller T, Czosnyka M, Timmer J, Hetzel A. Cerebral autoregulation in carotid artery occlusive disease assessed from spontaneous blood pressure fluctuations by the correlation coefficient index. Stroke. 2003;34(9):2138–44.

    Article  CAS  PubMed  Google Scholar 

  17. Intharakham K, Beishon L, Panerai RB, Haunton VJ, Robinson TG. Assessment of cerebral autoregulation in stroke: a systematic review and meta-analysis of studies at rest. J Cereb Blood Flow Metab. 2019;39(11):2105–16.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Naqvi J, Yap KH, Ahmad G, Ghosh J. Transcranial Doppler ultrasound: a review of the physical principles and major applications in critical care. Int J Vasc Med. 2013;2013:629378.

    PubMed  PubMed Central  Google Scholar 

  19. Brady KM, Lee JK, Kibler KK, et al. Continuous time-domain analysis of cerebrovascular autoregulation using near-infrared spectroscopy. Stroke. 2007;38(10):2818–25.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Rivera-Lara L, Geocadin R, Zorrilla-Vaca A, et al. Validation of near-infrared spectroscopy for monitoring cerebral autoregulation in comatose patients. Neurocrit Care. 2017;27(3):362–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zweifel C, Castellani G, Czosnyka M, et al. Continuous assessment of cerebral autoregulation with near-infrared spectroscopy in adults after subarachnoid hemorrhage. Stroke. 2010;41(9):1963–8.

    Article  PubMed  Google Scholar 

  22. Faraci FM, Brian JE Jr. Nitric oxide and the cerebral circulation. Stroke. 1994;25(3):692–703.

    Article  CAS  PubMed  Google Scholar 

  23. Novak V, Hajjar I. The relationship between blood pressure and cognitive function. Nat Rev Cardiol. 2010;7(12):686–98.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Hu K, Peng CK, Czosnyka M, Zhao P, Novak V. Nonlinear assessment of cerebral autoregulation from spontaneous blood pressure and cerebral blood flow fluctuations. Cardiovasc Eng. 2008;8(1):60–71.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Novak V, Yang AC, Lepicovsky L, Goldberger AL, Lipsitz LA, Peng CK. Multimodal pressure-flow method to assess dynamics of cerebral autoregulation in stroke and hypertension. Biomed Eng Online. 2004;3(1):39.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Machado MF, Muela HCS, Costa-Hong VA, et al. Evaluation of cerebral autoregulation performance in patients with arterial hypertension on drug treatment. J Clin Hypertens (Greenwich). 2020;22(11):2114–20.

    Article  CAS  Google Scholar 

  27. Panerai RB. Assessment of cerebral pressure autoregulation in humans—a review of measurement methods. Physiol Meas. 1998;19(3):305–38.

    Article  CAS  PubMed  Google Scholar 

  28. Spronk E, Sykes G, Falcione S, et al. Hemorrhagic transformation in ischemic stroke and the role of inflammation. Front Neurol. 2021;12:661955.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Eames PJ, Blake MJ, Dawson SL, Panerai RB, Potter JF. Dynamic cerebral autoregulation and beat to beat blood pressure control are impaired in acute ischaemic stroke. J Neurol Neurosurg Psychiatry. 2002;72(4):467–72.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Reinhard M, Roth M, Guschlbauer B, et al. Dynamic cerebral autoregulation in acute ischemic stroke assessed from spontaneous blood pressure fluctuations. Stroke. 2005;36(8):1684–9.

    Article  CAS  PubMed  Google Scholar 

  31. Castro P, Serrador JM, Rocha I, Sorond F, Azevedo E. Efficacy of cerebral autoregulation in early ischemic stroke predicts smaller infarcts and better outcome. Front Neurol. 2017;8:113.

    PubMed  PubMed Central  Google Scholar 

  32. Ma H, Guo ZN, Jin H, et al. Preliminary study of dynamic cerebral autoregulation in acute ischemic stroke: association with clinical factors. Front Neurol. 2018;9:1006.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Castro P, Azevedo E, Serrador J, Rocha I, Sorond F. Hemorrhagic transformation and cerebral edema in acute ischemic stroke: link to cerebral autoregulation. J Neurol Sci. 2017;372:256–61.

    Article  PubMed  Google Scholar 

  34. Immink RV, van Montfrans GA, Stam J, Karemaker JM, Diamant M, van Lieshout JJ. Dynamic cerebral autoregulation in acute lacunar and middle cerebral artery territory ischemic stroke. Stroke. 2005;36(12):2595–600.

    Article  PubMed  Google Scholar 

  35. Guo ZN, Liu J, Xing Y, et al. Dynamic cerebral autoregulation is heterogeneous in different subtypes of acute ischemic stroke. PLoS ONE. 2014;9(3):e93213.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Petersen NH, Ortega-Gutierrez S, Reccius A, Masurkar A, Huang A, Marshall RS. Dynamic cerebral autoregulation is transiently impaired for one week after large-vessel acute ischemic stroke. Cerebrovasc Dis. 2015;39(2):144–50.

    Article  PubMed  Google Scholar 

  37. Purkayastha S, Fadar O, Mehregan A, et al. Impaired cerebrovascular hemodynamics are associated with cerebral white matter damage. J Cereb Blood Flow Metab. 2014;34(2):228–34.

    Article  PubMed  Google Scholar 

  38. Tian G, Ji Z, Lin Z, Pan S, Yin J. Cerebral autoregulation is heterogeneous in different stroke mechanism of ischemic stroke caused by intracranial atherosclerotic stenosis. Brain Behav. 2021;11(1):e01907.

    Article  PubMed  Google Scholar 

  39. Ma H, Liu J, Lv S, et al. Dynamic cerebral autoregulation in embolic stroke of undetermined source. Front Physiol. 2020;11:557408.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Dohmen C, Bosche B, Graf R, et al. Identification and clinical impact of impaired cerebrovascular autoregulation in patients with malignant middle cerebral artery infarction. Stroke. 2007;38(1):56–61.

    Article  PubMed  Google Scholar 

  41. Sheriff F, Castro P, Kozberg M, et al. Dynamic cerebral autoregulation post endovascular thrombectomy in acute ischemic stroke. Brain Sci. 2020;10(9):641.

    Article  PubMed Central  Google Scholar 

  42. Meyer M, Juenemann M, Braun T, et al. Impaired cerebrovascular autoregulation in large vessel occlusive stroke after successful mechanical thrombectomy: a prospective cohort study. J Stroke Cerebrovasc Dis. 2020;29:104596.

    Article  PubMed  Google Scholar 

  43. Aries MJ, Elting JW, De Keyser J, Kremer BP, Vroomen PC. Cerebral autoregulation in stroke: a review of transcranial Doppler studies. Stroke. 2010;41(11):2697–704.

    Article  PubMed  Google Scholar 

  44. Petersen NH, Silverman A, Wang A, et al. Association of personalized blood pressure targets with hemorrhagic transformation and functional outcome after endovascular stroke therapy. JAMA Neurol. 2019;76:1256.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Oeinck M, Neunhoeffer F, Buttler KJ, et al. Dynamic cerebral autoregulation in acute intracerebral hemorrhage. Stroke. 2013;44(10):2722–8.

    Article  PubMed  Google Scholar 

  46. Reinhard M, Neunhoeffer F, Gerds TA, et al. Secondary decline of cerebral autoregulation is associated with worse outcome after intracerebral hemorrhage. Intensive Care Med. 2010;36(2):264–71.

    Article  PubMed  Google Scholar 

  47. Nakagawa K, Serrador JM, LaRose SL, Sorond FA. Dynamic cerebral autoregulation after intracerebral hemorrhage: a case-control study. BMC Neurol. 2011;11:108.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Ma H, Guo ZN, Liu J, Xing Y, Zhao R, Yang Y. Temporal course of dynamic cerebral autoregulation in patients with intracerebral hemorrhage. Stroke. 2016;47(3):674–81.

    Article  CAS  PubMed  Google Scholar 

  49. Ma H, Guo ZN, Sun X, et al. Hematoma volume is a predictive factor of disturbed autoregulation after spontaneous intracerebral hemorrhage. J Neurol Sci. 2017;382:96–100.

    Article  PubMed  Google Scholar 

  50. Xiong L, Tian G, Lin W, et al. Is dynamic cerebral autoregulation bilaterally impaired after unilateral acute ischemic stroke? J Stroke Cerebrovasc Dis. 2017;26(5):1081–7.

    Article  PubMed  Google Scholar 

  51. Jaeger M, Schuhmann MU, Soehle M, Nagel C, Meixensberger J. Continuous monitoring of cerebrovascular autoregulation after subarachnoid hemorrhage by brain tissue oxygen pressure reactivity and its relation to delayed cerebral infarction. Stroke. 2007;38(3):981–6.

    Article  PubMed  Google Scholar 

  52. Calviere L, Nasr N, Arnaud C, et al. Prediction of delayed cerebral ischemia after subarachnoid hemorrhage using cerebral blood flow velocities and cerebral autoregulation assessment. Neurocrit Care. 2015;23(2):253–8.

    Article  PubMed  Google Scholar 

  53. Soehle M, Czosnyka M, Pickard JD, Kirkpatrick PJ. Continuous assessment of cerebral autoregulation in subarachnoid hemorrhage. Anesth Anal. 2004;98(4):1133–9.

    Article  Google Scholar 

  54. Budohoski KP, Czosnyka M, Kirkpatrick PJ, et al. Bilateral failure of cerebral autoregulation is related to unfavorable outcome after subarachnoid hemorrhage. Neurocrit Care. 2015;22(1):65–73.

    Article  PubMed  Google Scholar 

  55. Guo ZN, Jin H, Sun H, et al. Antioxidant melatonin: potential functions in improving cerebral autoregulation after subarachnoid hemorrhage. Front Physiol. 2018;9:1146.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Conzen C, Becker K, Albanna W, et al. The acute phase of experimental subarachnoid hemorrhage: intracranial pressure dynamics and their effect on cerebral blood flow and autoregulation. Transl Stroke Res. 2019;10(5):566–82.

    Article  CAS  PubMed  Google Scholar 

  57. Santos GA, Petersen N, Zamani AA, et al. Pathophysiologic differences in cerebral autoregulation after subarachnoid hemorrhage. Neurology. 2016;86(21):1950–6.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Jaeger M, Soehle M, Schuhmann MU, Meixensberger J. Clinical significance of impaired cerebrovascular autoregulation after severe aneurysmal subarachnoid hemorrhage. Stroke. 2012;43(8):2097–101.

    Article  PubMed  Google Scholar 

  59. Otite F, Mink S, Tan CO, et al. Impaired cerebral autoregulation is associated with vasospasm and delayed cerebral ischemia in subarachnoid hemorrhage. Stroke. 2014;45(3):677–82.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Fontana J, Wenz H, Schmieder K, Barth M. Impairment of dynamic pressure autoregulation precedes clinical deterioration after aneurysmal subarachnoid hemorrhage. J Neuroimaging. 2016;26(3):339–45.

    Article  PubMed  Google Scholar 

  61. Chi NF, Hu HH, Wang CY, et al. Dynamic cerebral autoregulation is an independent functional outcome predictor of mild acute ischemic stroke. Stroke. 2018;49(11):2605–11.

    Article  PubMed  Google Scholar 

  62. Reinhard M, Rutsch S, Lambeck J, et al. Dynamic cerebral autoregulation associates with infarct size and outcome after ischemic stroke. Acta Neurol Scand. 2012;125(3):156–62.

    Article  CAS  PubMed  Google Scholar 

  63. Tian G, Ji Z, Huang K, Lin Z, Pan S, Wu Y. Dynamic cerebral autoregulation is an independent outcome predictor of acute ischemic stroke after endovascular therapy. BMC Neurol. 2020;20(1):189.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Nogueira RC, Lam MY, Llwyd O, et al. Cerebral autoregulation and response to intravenous thrombolysis for acute ischemic stroke. Sci Rep. 2020;10(1):10554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Chi NF, Hu HH, Chan L, et al. Impaired cerebral autoregulation is associated with poststroke cognitive impairment. Ann Clin Transl Neurol. 2020;7(7):1092–102.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Rynkowski CB, de Oliveira Manoel AL, Dos Reis MM, et al. Early transcranial doppler evaluation of cerebral autoregulation independently predicts functional outcome after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2019;31(2):253–62.

    Article  PubMed  Google Scholar 

  67. Budohoski KP, Czosnyka M, Smielewski P, et al. Monitoring cerebral autoregulation after subarachnoid hemorrhage. Acta Neurochir Suppl. 2016;122:199–203.

    Article  PubMed  Google Scholar 

  68. Liu G, Guo Z, Sun X, et al. Monitoring of the effect of cerebral autoregulation on delayed cerebral ischemia in patients with aneurysmal subarachnoid hemorrhage. World Neurosurg. 2018;118:e269–75.

    Article  PubMed  Google Scholar 

  69. Gaasch M, Schiefecker AJ, Kofler M, et al. Cerebral autoregulation in the prediction of delayed cerebral ischemia and clinical outcome in poor-grade aneurysmal subarachnoid hemorrhage patients. Crit Care Med. 2018;46(5):774–80.

    Article  PubMed  Google Scholar 

  70. Brooks FA, Ughwanogho U, Henderson GV, Black-Schaffer R, Sorond FA, Tan CO. The link between cerebrovascular hemodynamics and rehabilitation outcomes after aneurysmal subarachnoid hemorrhage. Am J Phys Med Rehabil. 2018;97(5):309–15.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Fontana J, Moratin J, Ehrlich G, et al. Dynamic autoregulatory response after aneurysmal subarachnoid hemorrhage and its relation to angiographic vasospasm and clinical outcome. Neurocrit Care. 2015;23(3):355–63.

    Article  PubMed  Google Scholar 

  72. Lang EW, Diehl RR, Mehdorn HM. Cerebral autoregulation testing after aneurysmal subarachnoid hemorrhage: the phase relationship between arterial blood pressure and cerebral blood flow velocity. Crit Care Med. 2001;29(1):158–63.

    Article  CAS  PubMed  Google Scholar 

  73. Silverman A, Kodali S, Strander S, et al. Deviation from personalized blood pressure targets is associated with worse outcome after subarachnoid hemorrhage. Stroke. 2019;50(10):2729–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Rasulo FA, Girardini A, Lavinio A, et al. Are optimal cerebral perfusion pressure and cerebrovascular autoregulation related to long-term outcome in patients with aneurysmal subarachnoid hemorrhage? J Neurosurg Anesthesiol. 2012;24(1):3–8.

    Article  PubMed  Google Scholar 

  75. Petersen NH, Silverman A, Strander SM, et al. Fixed compared with autoregulation-oriented blood pressure thresholds after mechanical thrombectomy for ischemic stroke. Stroke. 2020;51(3):914–21.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Eide PK, Sorteberg A, Bentsen G, Marthinsen PB, Stubhaug A, Sorteberg W. Pressure-derived versus pressure wave amplitude-derived indices of cerebrovascular pressure reactivity in relation to early clinical state and 12-month outcome following aneurysmal subarachnoid hemorrhage. J Neurosurg. 2012;116(5):961–71.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We sincerely thank Ms. Claire Levine, MS, ESL (Johns Hopkins University), for her diligent proofreading of this article. This article was prepared while Dr. Rebecca Gottesman was employed at the Johns Hopkins University School of Medicine. The opinions expressed in this article are the authors’ own and do not reflect the view of the National Institutes of Health, the Department of Health and Human Services, or the United States Government.

Funding

None.

Author information

Authors and Affiliations

Authors

Contributions

Drs. MAK and LRL had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the analysis. Study concept and design: MAK, SMC, LRL. Acquisition, analysis, or interpretation of data: MAK, LRL. Drafting of the manuscript: MAK, LRL. Critical revision of the manuscript for important intellectual content: MAK, SMC, RFG, JIS, LRL. Analysis: MAK, LRL. Study supervision: LRL.

Corresponding author

Correspondence to Mais Al-Kawaz.

Ethics declarations

Conflict of interest

Dr. Al-Kawaz, Dr. Cho, Dr. Suarez, and Dr. Rivera-Lara have nothing to disclose. Dr. Gottesman was a former associate editor for the journal Neurology but has no other disclosures.

Ethical Approval

This manuscript complies with all instructions to authors. The authorship requirements have been met and the final manuscript was approved by all authors. The manuscript has not been published elsewhere and is not under consideration by another journal. No IRB was required as this manuscript is a review article. This study also conforms to the Preferred Reporting Items for Systematic Reviews (PRISMA) Guidelines.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al-Kawaz, M., Cho, SM., Gottesman, R.F. et al. Impact of Cerebral Autoregulation Monitoring in Cerebrovascular Disease: A Systematic Review. Neurocrit Care 36, 1053–1070 (2022). https://doi.org/10.1007/s12028-022-01484-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12028-022-01484-5

Keywords

Navigation